Bone marrow mesenchymal stem cells-derived exosomes containing miR-539-5p inhibit pyroptosis through NLRP3/caspase-1 signalling to alleviate inflammatory bowel disease

Inflamm Res. 2022 Aug;71(7-8):833-846. doi: 10.1007/s00011-022-01577-z. Epub 2022 May 30.

Abstract

Background: Exosomes derived from bone mesenchymal stem cells (BMSCs) are potential candidates for inflammatory bowel disease (IBD) treatment. The present study investigated the therapeutic effect and potential mechanism of BMSCs-derived exosomes on pyroptosis in IBD.

Methods: We induced IBD in mice and cell models through dextran sulfate sodium (DSS) and LPS, respectively. The mRNA and protein expression levels were assessed by qRT-PCR, Western blotting, IF and IHC. The concentrations of IL-1β, IL-18 and TNFα were assessed using ELISA. ROS levels were determined using DCFH-DA staining. Cell proliferation of mIECs was analysed using an MTT assay. In addition, a flow cytometry assay was performed to detect pyroptosis. Finally, the binding relationship between miR-539-5p and NLRP3 was verified by a dual luciferase reporter gene assay.

Results: Our results revealed that intraperitoneal injection of BMSCs-derived exosomes inhibited DSS-induced pyroptosis as well as IBD symptoms in mice. In addition, BMSCs-derived exosome treatment suppressed pyroptosis, ROS levels and the concentrations of proinflammatory cytokines (IL-1β, IL-18 and TNFα) in LPS-treated mIECs in a miR-539-5p-dependent manner. Further research found that miR-539-5p suppressed NLRP3 expression in mIECs by directly targeting NLRP3. As expected, pyroptosis in LPS-treated mIECs was significantly reduced by NLRP3 knockdown. In addition, NLRP3 silencing restored the inhibitory effect of exosomes derived from BMSCs transfected with miR-539-5p inhibitor on pyroptosis in LPS-treated mIECs.

Conclusion: The present study demonstrated that BMSCs-derived exosomal miR-539-5p suppresses pyroptosis through NLRP3/caspase-1 signalling to inhibit IBD progression.

Keywords: Bone mesenchymal stem cells; Exosome; Inflammatory bowel disease; Pyroptosis; miR-539-5p.

MeSH terms

  • Animals
  • Caspase 1 / metabolism
  • Exosomes*
  • Inflammatory Bowel Diseases* / therapy
  • Interleukin-18 / genetics
  • Interleukin-18 / metabolism
  • Lipopolysaccharides / pharmacology
  • Mesenchymal Stem Cells* / metabolism
  • Mice
  • MicroRNAs* / metabolism
  • NLR Family, Pyrin Domain-Containing 3 Protein / genetics
  • NLR Family, Pyrin Domain-Containing 3 Protein / metabolism
  • Pyroptosis
  • Reactive Oxygen Species / metabolism
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Interleukin-18
  • Lipopolysaccharides
  • MicroRNAs
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Nlrp3 protein, mouse
  • Reactive Oxygen Species
  • Tumor Necrosis Factor-alpha
  • Caspase 1